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Altered access to beneficial mutations slows adaptation and biases fixed mutations in diploids

Nature Ecology & Evolutionvolume 2pages882889 (2018) | Download Citation

Abstract

Ploidy varies considerably in nature. However, our understanding of the impact of ploidy on adaptation is incomplete. Many microbial evolution experiments characterize adaptation in haploid organisms, but few focus on diploid organisms. Here, we perform a 4,000-generation evolution experiment using diploid strains of the yeast Saccharomyces cerevisiae. We show that the rate of adaptation and spectrum of beneficial mutations are influenced by ploidy. Haldane’s sieve effectively alters access to recessive beneficial mutations in diploid populations, leading to a slower rate of adaptation and a spectrum of beneficial mutations that is shifted towards dominant mutations. Genomic position also has an important role, as the prevalence of homozygous mutations is largely dependent on their proximity to a recombination hotspot. Our results demonstrate key aspects of diploid adaptation that have previously been understudied and provide support for several proposed theories.

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Acknowledgements

We thank M. Remillard (Princeton University) for providing strains; A. Nguyen and M. Desai (Harvard University) for providing the plasmid with mating-type-specific selectable markers; A. Selmecki, K. Fisher and R. Vignogna for their comments on the manuscript. This work was supported by the Charles E. Kaufman Foundation of The Pittsburgh Foundation.

Author information

Affiliations

  1. Department of Biological Sciences, Lehigh University, Bethlehem, PA, USA

    • Daniel A. Marad
    • , Sean W. Buskirk
    •  & Gregory I. Lang

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Contributions

G.I.L. designed the project. D.A.M. performed the experiments. S.W.B. and D.A.M. performed the sequencing analysis pipeline. D.A.M. and G.I.L. analysed the data and wrote the manuscript.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Gregory I. Lang.

Supplementary information

  1. Supplementary Information

    Supplementary Figs. 1–8, Supplementary Table 1

  2. Life Sciences Reporting Summary

  3. Supplementary Table 2

    Mutations detected in two clones each from 24 diploid populations

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DOI

https://doi.org/10.1038/s41559-018-0503-9